Intraguild predation (IGP) is a ubiquitous, important and common interaction that occurs in aphidophagous guilds. The effects of extraguild prey (EGP, i.e., aphids) density, predator life stage combinations and duration of the interaction on the level, asymmetry and direction of intraguild predation between lacewing Chrysoperla carnea and ladybird Hippodamia variegata were examined in simple laboratory arena and more complex microcosm environment. Three initial densities of 50, 150 and 400 Aphis fabae third instar nymphs and a control without aphids were provided to six combinations of predator life stages (2nd and 3rd larval instars of lacewing and 3rd and 4th instars and adult females of ladybird). The remaining aphid density and occurrence of IGP were checked after 24, 48 and 72 h. The IGP intensity (IGP level, IL) was similar in the simple arena (reaching 0.6 between larvae in absence of EGP and 0.3 between lacewing larvae and ladybird females) and microcosm environment (0.3 without EGP). In both environments, increasing EGP density lowered IL according to negative exponential relationship. IGP was asymmetric (general average asymmetry was 0.82 in simple arena and 0.93 in microcosm, the difference was not significant) and mostly in favour of larvae of C. carnea, except in the combination of 2nd larvae of C. carnea with the 4th larvae and adults of H. variegata. The direction of IGP, but not other characteristics, partially changed during the duration of the experiment. The incidence of IGP interactions among aphid predators under real conditions and its consequences on aphid biological control are discussed.

Biology Centre Czech Academy of Sciences Institute of Entomology Branišovská 31 37005 České Budějovice Czech Republic

Department of Plant Protection College of Agriculture Razi University Kermanshah 6714414971 Iran

Department of Plant Protection Faculty of Agriculture Bu Ali Sina University Hamedan 6517838695 Iran

Faculty of Science University of South Bohemia Branišovská 1760 37005 České Budějovice Czech Republic

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Polis G.A., Myers C.A., Holt R.D. The ecology and evolution of intraguild predation: Potential competitors that eat each other. Annu. Rev. Ecol. Syst. 1989;20:297–330. doi: 10.1146/annurev.es.20.110189.001501. DOI

Felix S., Soares A.O. Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): The role of body weight. Eur. J. Entomol. 2004;101:237–242. doi: 10.14411/eje.2004.032. DOI

Polis G.A., Holt R.D. Intraguild Predation: The dynamics of complex trophic interactions. Trends Ecol. Evol. 1992;7:151–155. doi: 10.1016/0169-5347(92)90208-S. PubMed DOI

Holt R.D., Polis G.A. A Theoretical framework for intraguild predation. Am. Nat. 1997;149:745–764. doi: 10.1086/286018. DOI

Křivan V., Diehl S. Adaptive omnivory and species coexistence in tri-trophic food webs. Theor. Popul. Biol. 2005;67:85–99. doi: 10.1016/j.tpb.2004.09.003. PubMed DOI

Rosenheim J.A., Limburg D.D., Colfer R. Impact of generalist predators on a biological control agent, Chrysoperla carnea: Direct observation. Ecol. Appl. 1999;9:409–417. doi: 10.1890/1051-0761(1999)009[0409:IOGPOA]2.0.CO;2. DOI

Madadi H., Enkegaard A., Brodsgaard H.F., Kharrazi-Pakdel A., Ashouri A., Mohaghegh-Neishabouri J. Interactions between Orius albidipennis (Heteroptera: Anthocoridae) and Neoseiulus cucumeris (Acari: Phytoseiidae): Effects of host plants under microcosm condition. Biol. Control. 2009;50:137–142. doi: 10.1016/j.biocontrol.2009.03.015. DOI

Ingles B., De Clercq P. Effect of size, extraguild prey and habitat complexity on intraguild interactions: A case study with the invasive ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus. Biocontrol. 2011;56:871–882. doi: 10.1007/s10526-011-9363-9. DOI

Trotta V., Duran Prieto J., Fanti P., Battaglia D. Prey abundance and intraguild predation between Adalia bipunctata (Coleoptera: Coccinellidae) and Macrolophus pygmaeus (Hemiptera: Miridae) Eur. J. Entomol. 2015;112:862–865. doi: 10.14411/eje.2015.080. DOI

Lucas E. Intraguild predation among aphidophagous predators. Eur. J. Entomol. 2005;102:351–364. doi: 10.14411/eje.2005.052. DOI

Rondoni G., Onofri A., Ricci C. Differential susceptibility in a specialised aphidophagous ladybird, Platynaspis luteorubra (Coleoptera: Coccinellidae), facing intraguild predation by exotic and native generalist predators. Biocontrol Sci. Techn. 2012;22:1334–1350. doi: 10.1080/09583157.2012.726607. DOI

Nedvěd O., Fois X., Ungerova D., Kalushkov P. Alien vs. predator – the native lacewing Chrysoperla carnea is the superior intraguild predator in trials against the invasive ladybird Harmonia axyridis. Bull. Insectol. 2013;66:73–78.

Tavoosi Ajvad F., Madadi H., Gharali B. Influence of intraguild predation between Episyrphus balteatus and Hippodamia variegata on their prey. Arch. Phytopathol. Plant Prot. 2014;47:106–112. doi: 10.1080/03235408.2013.804249. DOI

Wells P.M., Baverstock J., Clark S.J., Giggins F.M., Roy H.E., Pell J.K. Determining the effects of life stage, shared prey density and host plant on intraguild predation of a native lacewing (Chrysoperla carnea) by an invasive coccinellid (Harmonia axyridis) Biocontrol. 2017;62:373–384. doi: 10.1007/s10526-016-9775-7. DOI

Rosenheim J.A., Wilhoit L.R. Predators that eat other predators disrupt cotton aphid control. Calif. Agr. 1993;47:7–9. doi: 10.3733/ca.v047n05p7. DOI

Pappas M.L., Broufas G.D., Koveos D.S. Chrysopid predators and their role in biological control. J. Entomol. 2011;8:301–326. doi: 10.3923/je.2011.301.326. DOI

Guncan A., Yoldas Z., Madanlar N. Studies on the aphids (Hemiptera: Aphididae) and their natural enemies on peach orchards in Izmir. Turk. J. Entomol. 2010;34:399–408.

Saeidi K., Adam N.A. A survey on pest insect fauna of safflower fields in the Iranian Province of Kohgiloyeh and Boyerahmad. Afr. J. Agric. Res. 2011;6:4441–4446.

Sengonca C., Frings B. Interference and competitive bahaviour of the aphid predators, Chrysoperla carnea and Coccinella septempunctata in the laboratory. Entomophaga. 1985;30:245–251. doi: 10.1007/BF02372225. DOI

Phoofolo M.W., Obrycki J.J. Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomol.Exp. Appl. 1998;89:47–55. doi: 10.1046/j.1570-7458.1998.00380.x. DOI

Michaud J.P., Grant A.K. Intraguild predation among ladybeetles and a green lacewings: Do the larval spines of Curinus coeruleus (Coleoptera: Coccinellidae) serve a defensive function? Bull. Entomol. Res. 2003;93:499–505. doi: 10.1079/BER2003269. PubMed DOI

Santi F., Maini S. Predation upon Adalia bipunctata and Harmonia axyridis eggs by Chrysoperla carnea larvae and Orius laevigatus adults. Bull. Insectol. 2006;59:53–58.

Finke D.L., Denno R.F. Spatial refuge from intraguild predation: Implications for prey suppression and trophic cascades. Oecologia. 2006;149:265–275. doi: 10.1007/s00442-006-0443-y. PubMed DOI

Lucas E., Rosenheim A.J. Influence of extraguild prey density on intraguild predation by heteropteran predators: A review of the evidence and a case study. Biol. control. 2011;56:61–67. doi: 10.1016/j.biocontrol.2011.05.010. DOI

Noppe C., Michaud J.P., De Clercq P. Intraguild Predation between lady beetles and lacewings: Outcomes and consequences vary with focal prey and arena of interaction. Ann. Entomol. Soc. Am. 2012;4:562–571. doi: 10.1603/AN11165. DOI

Lucas E., Coderre D., Brodeur J. Intraguild predation among aphid predators: Characterization and influence of extraguild prey density. Ecology. 1998;79:1084–1092. doi: 10.1890/0012-9658(1998)079[1084:IPAAPC]2.0.CO;2. DOI

De Clercq P., Peeters I., Vergauwe G., Thas O. Interaction between Podisus maculiventris and Harmonia axyridis two predators used in augmentative biological control in greenhouse crops. Biocontrol. 2003;48:39–55. doi: 10.1023/A:1021219714684. DOI

Finke D.L., Denno R.F. Intraguild predation diminished in complex-structured vegetation: Implications for prey suppression. Ecology. 2002;83:643–652. doi: 10.1890/0012-9658(2002)083[0643:IPDICS]2.0.CO;2. DOI

Zarei M., Madadi H., Zamani A.A., Nedvěd O. Predation rate of competing Chrysoperla carnea (Neuroptera: Chrysopidae) and Hippodamia variegata (Coleoptera: Coccinellidae) on Aphis fabae (Sternorrhyncha: Aphididae) at various prey densities and arena complexities. Bull. Insectol. 2019;72:273–280. PubMed

TIBCO Software Inc. Statistica (Data Analysis Software System), Version 13. [(accessed on 9 January 2020)];2017 Available online: http://statistica.io.

Noia M., Borges I., Soares A.O. Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): The role of intra and extraguild prey densities. Biol. Control. 2008;46:140–146. doi: 10.1016/j.biocontrol.2008.03.004. DOI

Rondoni G., Ielo F., Ricci C., Conti E. Intraguild predation responses in two aphidophagous coccinellids identify differences among juvenile stages and aphid densities. Insects. 2014;5:974–983. doi: 10.3390/insects5040974. PubMed DOI PMC

Janssen A., Sabelis M.W., Magalhaes S., Montserrat M., Van der Hammen T. Habitat structure affects intraguild predation. Ecology. 2007;88:2713–2719. doi: 10.1890/06-1408.1. PubMed DOI

South J., McCard M., Khosa D., Mofu L., Madzivanzira T.C., Dick J.T.A., Weyl O.L.F. The effect of prey identity and substrate type on the functional response of a globally invasive crayfish. Neobiota. 2019;52:9–24. doi: 10.3897/neobiota.52.39245. DOI

Janssen A., Montserrat M., HilleRis Lambers R., de Roos A.M., Pallini A., Sabelis M.W. Intraguild predation usually does not disrupt biological control. In: Brodeur J., Boivin G., editors. Trophic and Guild in Biological Interactions Control. Progress in Biological Control. Volume 3. Springer; Dordrecht, The Netherland: 2006. pp. 21–44.

Chang G.C. Comparison of single versus multiple species of generalist predators for biological control. Biol. Control. 1996;25:207–212. doi: 10.1093/ee/25.1.207. DOI

Snyder W.E., Ballard S.N., Yang S., Clevenger G.M., Miller T.D., Ahn J.J., Hatten T.D., Berryman A.A. Complementary biocontrol of aphids by the ladybird beetle Harmonia axyridis and the parasitoid Aphelinus asychis on greenhouse roses. Biol. Control. 2004;30:229–235. doi: 10.1016/j.biocontrol.2004.01.012. DOI